Cited by 315Evolution and Paleontology StudiesMorphological variations and asymmetryGenomics and Phylogenetic Studies

The DOI matches its Crossref record; 127 of the 127 references it cites were found in a registry or an index; 16 of the 68 sources its claims cite were checked for support.

Rethinking phylogenetic comparative methods

Open access
Uyeda, Josef C, Zenil-Ferguson, Rosana, Pennell, Matthew W·2018·Systematic Biology

Published version of a preprint

Abstract

As a result of the process of descent with modification, closely related species tend to be similar to one another in a myriad different ways. In statistical terms, this means that traits measured on one species will not be independent of traits measured on others. Since their introduction in the 1980s, phylogenetic comparative methods (PCMs) have been framed as a solution to this problem. In this article, we argue that this way of thinking about PCMs is deeply misleading. Not only has this sowed widespread confusion in the literature about what PCMs are doing but has led us to develop methods that are susceptible to the very thing we sought to build defenses against-unreplicated evolutionary events. Through three Case Studies, we demonstrate that the susceptibility to singular events is indeed a recurring problem in comparative biology that links several seemingly unrelated controversies. In each Case Study, we propose a potential solution to the problem. While the details of our proposed solutions differ, they share a common theme: unifying hypothesis testing with data-driven approaches (which we term "phylogenetic natural history") to disentangle the impact of singular evolutionary events from that of the factors we are investigating. More broadly, we argue that our field has, at times, been sloppy when weighing evidence in support of causal hypotheses. We suggest that one way to refine our inferences is to re-imagine phylogenies as probabilistic graphical models; adopting this way of thinking will help clarify precisely what we are testing and what evidence supports our claims.

Overview

AI snapshot

Written from the paper’s full text.

TL;DR

The paper argues that phylogenetic comparative methods are commonly mischaracterized as solving nonindependence and are instead vulnerable to singular, unreplicated evolutionary events that can generate spurious associations. Through three case studies it recommends combining hypothesis testing with data-driven “phylogenetic natural history” and using graphical models to clarify causal inference.

Key findings

  • Across continuous and discrete comparative methods, a single unreplicated shift can drive significant associations; in Felsenstein’s worst-case simulations, as shift variance relative to BM variance increases, the proportion of significant contrast regressions increases dramatically (each point represents 200 simulations for a fixed phylogeny).
  • Reanalysis of the Scales et al. (2009) data set of fast glycolytic muscle fiber fraction across 22 squamate lizards found the original predator-escape (PE) hypothesis was 13.0 AICc units better than the next closest model (FMPE), but a Bayesian mixture with RJMCMC gave intermediate weight to PE on empirical data and recovered only a single highly supported shift on the stem branch of *Phrynosoma*; combined analysis gave strongest support to a *Phrynosoma*-only model, intermediate support to PE, and little support to the reversible-jump component.
  • For discrete traits under Darwin’s scenario, Pagel’s correlation test statistic reduces to \(D = 2(\ln(T)-\ln(t))\), so support for the dependent model increases with total tree length; simulations on 20-taxon trees matched this prediction.
  • The authors recommend unifying hypothesis testing with data-driven “phylogenetic natural history” and rendering phylogenies as probabilistic graphical models/Bayesian networks to clarify causal assumptions.

Methods

  • Conceptual synthesis with three case studies; no single empirical data set spans all analyses.
  • Case I simulations used a two-clade phylogeny (unresolved or Yule fully bifurcating), two traits under independent Brownian motion with \(\sigma^2 = 1\), and a singular event on a stem branch drawn from a multivariate normal with uncorrelated equal variances that were a scalar multiple of \(\sigma^2\); Case III derived Pagel’s test under Darwin’s scenario and simulated 20-taxon trees in diversitree with irreversible transitions on one randomly chosen internal branch, constrained vs. unconstrained Pagel models, root state 0, and loss rates 0.
  • Case II built a Bayesian mixture model on the R package bayou, reanalyzing the Scales et al. (2009) 22-squamate data set and simulated data sets; expected trait values were a weighted average of a fixed PE regime painting and an RJMCMC-estimated shift configuration, with a truncated Poisson prior on number of shifts (mean 0.5, maximum 10) and a symmetric beta(0.8, 0.8) prior on the weight parameter.

Limitations

  • Stated by the authors: the “singular events” model is primarily illustrative; fitting realistic cases requires estimating the location and number of events; there is no one-size-fits-all solution; many details remain to be worked out and alternative paths were not considered.
  • Stated by the authors: in Case II, vague priors on the number and location of shifts in the reversible-jump analysis reward correctly guessing which branch contains a shift; ascertainment bias is likely prevalent; Darwin’s scenario is a boundary case, and the derivation’s assumptions differ slightly from available software.
  • Evident from the text: Case II is limited to one 22-species lizard data set plus simulated data sets, and Case III’s analytical result assumes traits were selected without first looking at their phylogenetic distribution—a condition the authors say is rarely met.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1093/sysbio/syy031

Cites

127 of 127 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Verification

Claims the paper makes

71 Own interpretation · 24 No full text of the sources · 18 No basis given · 16 Own result · 5 Supported so far · 5 Partly supported · 3 Supported · 2 Sources not found · 2 Not checked yet · accuracy not yet measured

Show all 90 claims

  • Probably not a substantial claim. 27
  • It may state two separate claims as one. 35
56 of 56
  • The paper relies on this without support.

    Descent with modification causes closely related species to be similar to one another in many traits.

    “As a result of the process of descent with modification, closely related species tend to be similar to one another in a myriad different ways.”
  • The authors state this as an assumption.

    Trait correlations can result from a single random shift drawn from a different distribution than the one used to model trait evolution across the rest of the branches.

    “We can do so by including another phylogenetically plausible model: that trait correlations result from a single random shift, drawn from a different distribution than the one used to model trait evolution across the rest of the branches.”
  • The authors state this as an assumption.

    The macroevolutionary optimum of a particular species is a weighted average of past regimes, as is typical in all OU models with discrete shifts in regimes.

    “we consider the macroevolutionary optimum of a particular species to be a weighted average of past regimes, as is typical in all OU models with discrete shifts in regimes (Butler and King 2004;Beaulieu et al. 2012)”
  • The authors state this as an assumption.

    The traits were selected for study without first looking at their phylogenetic distribution.

    “we assume that the traits were selected for study without first looking at their phylogenetic distribution, a condition that we (as well as Maddison and FitzJohn 2015) suspect is rarely met in practice”
  • The authors state this as an assumption.

    The likelihood of evolving these traits at all is quite small.

    “we can make the assumption that the likelihood of evolving these traits at all is quite small”
  • The authors state this as an assumption.

    Under Markovian assumptions, replaying the tape of life will likely lead to many worlds where milk and middle ear bones don't exist at all.

    “In other words, replaying the tape of life, under Markovian assumptions, will likely lead to many worlds where milk and middle ear bones don't exist at all.”
  • The authors state this as an assumption.

    The rates of gain of the traits are so low that only one shift is ever observed.

    “Particularly, we assume that the rates of gain of the traits are so low that only one shift is ever observed.”
  • The authors state this as an assumption.

    Ancestors are causes of descendants, and not vice versa.

    “the nature of phylogenies allows us to assume that ancestors are causes of descendants, and not vice versa”
  • The authors state this as an assumption.

    Body size influences migratory behavior (in the illustrative example).

    “If we assume that body size influences migratory behavior”
  • The authors state this as an assumption.

    Migratory behavior causes changes in body size (in the illustrative example).

    “if migratory behavior causes changes in body size”
  • The authors state this as an assumption.

    The rates of gain of the traits are so low that only one shift is ever observed (in the Figure 6 analysis).

    “we assume that the rates of gain of the traits are so low that only one shift is ever observed”
11 of 11

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Citations

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Metadata

Authors
Uyeda, J. C., Zenil-Ferguson, R., & Pennell, M. W.
Affiliations
  • Virginia Tech (US)
  • Department of Biological Sciences, University of Idaho, 875 Perimeter Drive, Moscow, ID 83844 USA
  • University of British Columbia (CA)
Corresponding author
Uyeda, Josef C
Venue
Systematic Biology
Published
2018-04-25
Volume
67
Issue
6
Pages
1091-1109
ISSN
  • 1063-5157 (ISSN-L)
  • 1076-836X
OpenAlex
W2951967147
Cited by
313
References
113
Citations by year
2026: 23 · 2025: 40 · 2024: 39 · 2023: 53 · 2022: 37 · 2021: 40 · 2020: 24 · 2019: 39 · 2018: 16
FWCI
22.03
Type
journal article
Language
en
Open access
Locations
  • Systematic Biology (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
  • PubMed (publishedVersion)
Funders
  • NSERC Discovery
  • NSF (DEB-1208912, DBI-1661516)
Topics
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Morphological variations and asymmetry
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
phylogenetic comparative analysis, hypothesis testing, causal inference, probabilistic graphical models, phylogeny, comparative biology
MeSH terms
Classification, Phylogeny

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